Exploring the Siderophore Portfolio for Mass Spectrometry-Based Diagnosis of Scedosporiosis and Lomentosporiosis
Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
39524635
PubMed Central
PMC11541790
DOI
10.1021/acsomega.4c08257
Knihovny.cz E-zdroje
- Publikační typ
- časopisecké články MeSH
Scedosporium apiospermum and Lomentospora prolificans secrete siderophores (iron scavengers) during hyphal proliferation. Siderophores are virulence factors and potential clinical biomarkers of invasive scedosporiosis and lomentosporiosis. Both strains secreted a uniform spectrum of siderophores, including coprogen B (CopB), N α-methyl-coprogen B, dimethyl-coprogen, and ferricrocin, with N α-methyl-coprogen B being the fastest secreted and most abundant coprogen. Under iron and zinc restriction, reflecting a nutrient-limited host environment, L. prolificans secreted 45 times more CopB than did S. apiospermum, presumably contributing to its higher virulence. This robust mobilization of CopB was further enhanced by zinc surplus. Additionally, two novel cyclic peptides, Scedocyclin A and B, were characterized inScedosporium boydii using the de novo sequencing tool CycloBranch. Utilizing matrix-assisted laser desorption/ionization, the portfolio of coprogens detected had limits of detection and quantitation of 4.9 and 14.6 fmol/spot in complex matrices, respectively, making them strong candidates for the next-generation, routine diagnosis of invasive scedosporiosis and lomentosporiosis through the Biotyper siderotyping.
Zobrazit více v PubMed
WHO fungal priority pathogens list to guide research, development and public health action. https://www.who.int/publications/i/item/9789240060241 (accessed Dec 9 , 2023).
Hoenigl M.; Salmanton-Garcia J.; Walsh T. J.; Nucci M.; Neoh C. F.; Jenks J. D.; Lackner M.; Sprute R.; Al-Hatmi A. M. S.; Bassetti M.; Carlesse F.; Freiberger T.; Koehler P.; Lehrnbecher T.; Kumar A.; Prattes J.; Richardson M.; Revankar S.; Slavin M. A.; Stemler J.; Spiess B.; Taj-Aldeen S. J.; Warris A.; Woo P. C. Y.; Young J. A. H.; Albus K.; Arenz D.; Arsic-Arsenijevic V.; Bouchara J. P.; Chinniah T. R.; Chowdhary A.; de Hoog G. S.; Dimopoulos G.; Duarte R. F.; Hamal P.; Meis J. F.; Mfinanga S.; Queiroz-Telles F.; Patterson T. F.; Rahav G.; Rogers T. R.; Rotstein C.; Wahyuningsih R.; Seidel D.; Cornely O. A. Global guideline for the diagnosis and management of rare mould infections: an initiative of the European Confederation of Medical Mycology in cooperation with the International Society for Human and Animal Mycology and the American Society for Microbiology. Lancet Infect. Dis. 2021, 21 (8), e246–e257. 10.1016/S1473-3099(20)30784-2. PubMed DOI
Ramirez-Garcia A.; Pellon A.; Rementeria A.; Buldain I.; Barreto-Bergter E.; Rollin-Pinheiro R.; de Meirelles J. V.; Xisto M.; Ranque S.; Havlicek V.; Vandeputte P.; Govic Y. L.; Bouchara J. P.; Giraud S.; Chen S.; Rainer J.; Alastruey-Izquierdo A.; Martin-Gomez M. T.; Lopez-Soria L. M.; Peman J.; Schwarz C.; Bernhardt A.; Tintelnot K.; Capilla J.; Martin-Vicente A.; Cano-Lira J.; Nagl M.; Lackner M.; Irinyi L.; Meyer W.; de Hoog S.; Hernando F. L. Scedosporium and Lomentospora: an updated overview of underrated opportunists. Med. Mycol. 2018, 56, 102–125. 10.1093/mmy/myx113. PubMed DOI
Mello T. P.; Oliveira S. S. C.; Branquinha M. H.; Santos A. L. S. Decoding the antifungal resistance mechanisms in biofilms of emerging, ubiquitous and multidrug-resistant species belonging to the Scedosporium/Lomentospora genera. Med. Mycol. 2022, 60 (6), myac036.10.1093/mmy/myac036. PubMed DOI
Guegan H.; Poirier W.; Ravenel K.; Dion S.; Delabarre A.; Desvillechabrol D.; Pinson X.; Sergent O.; Gallais I.; Gangneux J. P.; Giraud S.; Gastebois A. Deciphering the role of PIG1 and DHN-melanin in Scedosporium apiospermum conidia. J. Fungi 2023, 9 (2), 134.10.3390/jof9020134. PubMed DOI PMC
Mello T. P.; Bittencourt V. C. B.; Liporagi-Lopes L. C.; Aor A. C.; Branquinha M. H.; Santos A. L. S. Insights into the social life and obscure side of Scedosporium/Lomentospora species: ubiquitous, emerging and multidrug-resistant opportunistic pathogens. Fungal Bio. Rev. 2019, 33 (1), 16–46. 10.1016/j.fbr.2018.07.002. DOI
Toth E. J.; Nagy G. R.; Homa M.; Abrok M.; Kiss I. E.; Nagy G.; Bata-Csorgo Z.; Kemeny L.; Urban E.; Vagvolgyi C.; Papp T. Recurrent Scedosporium apiospermum mycetoma successfully treated by surgical excision and terbinafine treatment: a case report and review of the literature. Ann. Clin. Microbiol. Antimicrob. 2017, 16 (1), 31.10.1186/s12941-017-0195-z. PubMed DOI PMC
Schwarz C.; Brandt C.; Antweiler E.; Krannich A.; Staab D.; Schmitt-Grohe S.; Fischer R.; Hartl D.; Thronicke A.; Tintelnot K. Prospective multicenter German study on pulmonary colonization with Scedosporium/Lomentospora species in cystic fibrosis: epidemiology and new association factors. PLoS One 2017, 12 (2), e017148510.1371/journal.pone.0171485. PubMed DOI PMC
Seidel D.; Meissner A.; Lackner M.; Piepenbrock E.; Salmanton-Garcia J.; Stecher M.; Mellinghoff S.; Hamprecht A.; Duran Graeff L.; Kohler P.; Cheng M. P.; Denis J.; Chedotal I.; Chander J.; Pakstis D. L.; Los-Arcos I.; Slavin M.; Montagna M. T.; Caggiano G.; Mares M.; Trauth J.; Aurbach U.; Vehreschild M.; Vehreschild J. J.; Duarte R. F.; Herbrecht R.; Wisplinghoff H.; Cornely O. A. Prognostic factors in 264 adults with invasive Scedosporium spp. and Lomentospora prolificans infection reported in the literature and FungiScope. Crit. Rev. Microbiol. 2019, 45 (1), 1–21. 10.1080/1040841X.2018.1514366. PubMed DOI
Sedlacek L.; Graf B.; Schwarz C.; Albert F.; Peter S.; Wurstl B.; Wagner S.; Klotz M.; Becker A.; Haase G.; Laniado G.; Kahl B.; Suerbaum S.; Seibold M.; Tintelnot K. Prevalence of Scedosporium species and Lomentospora prolificans in patients with cystic fibrosis in a multicenter trial by use of a selective medium. J. Cyst. Fibros. 2015, 14 (2), 237–241. 10.1016/j.jcf.2014.12.014. PubMed DOI
Pham T.; Giraud S.; Schuliar G.; Rougeron A.; Bouchara J. P. Scedo-Select III: a new semi-selective culture medium for detection of the Scedosporium apiospermum species complex. Med. Mycol. 2015, 53 (5), 512–519. 10.1093/mmy/myv015. PubMed DOI
Gilgado F.; Cano J.; Gené J.; Guarro J. Molecular phylogeny of the Pseudallescheria boydii species complex: proposal of two new species. J. Clin. Microbiol. 2005, 43 (10), 4930–4942. 10.1128/JCM.43.10.4930-4942.2005. PubMed DOI PMC
Mina S.; Staerck C.; Marot A.; Godon C.; Calenda A.; Bouchara J. P.; Fleury M. J. J. Scedosporium boydii CatA1 and SODC recombinant proteins, new tools for serodiagnosis of Scedosporium infection of patients with cystic fibrosis. Diagn. Microbiol. Infect. Dis. 2017, 89 (4), 282–287. 10.1016/j.diagmicrobio.2017.08.013. PubMed DOI
Martin-Souto L.; Buldain I.; Areitio M.; Aparicio-Fernandez L.; Antoran A.; Bouchara J. P.; Martin-Gomez M. T.; Rementeria A.; Hernando F. L.; Ramirez-Garcia A. ELISA test for the serological detection of Scedosporium/Lomentospora in cystic fibrosis patients. Front. Cell. Infect. Microbiol. 2020, 10, 602089.10.3389/fcimb.2020.602089. PubMed DOI PMC
Pini P.; Venturelli C.; Girardis M.; Forghieri F.; Blasi E. Prognostic potential of the panfungal marker (1 → 3)-β-D-glucan in invasive mycoses patients. Mycopathologia 2019, 184 (1), 147–150. 10.1007/s11046-018-0282-5. PubMed DOI
Keller N. P. Fungal secondary metabolism: regulation, function and drug discovery. Nat. Rev. Microbiol. 2019, 17 (3), 167–180. 10.1038/s41579-018-0121-1. PubMed DOI PMC
Macheleidt J.; Mattern D. J.; Fischer J.; Netzker T.; Weber J.; Schroeckh V.; Valiante V.; Brakhage A. A. Regulation and role of fungal secondary metabolites. Annu. Rev. Genet. 2016, 50, 371–392. 10.1146/annurev-genet-120215-035203. PubMed DOI
Kriegl L.; Havlicek V.; Dichtl K.; Egger M.; Hoenigl M. Siderophores: a potential role as a diagnostic for invasive fungal disease. Curr. Opin. Infect. Dis. 2022, 35 (6), 485–492. 10.1097/QCO.0000000000000862. PubMed DOI
Happacher I.; Aguiar M.; Yap A.; Decristoforo C.; Haas H. Fungal siderophore metabolism with a focus on Aspergillus fumigatus: impact on biotic interactions and potential translational applications. Essays Biochem. 2023, 67 (5), 829–842. 10.1042/EBC20220252. PubMed DOI PMC
Luptakova D.; Patil R. H.; Dobias R.; Stevens D. A.; Pluhacek T.; Palyzova A.; Kanova M.; Navratil M.; Vrba Z.; Hubacek P.; Havlicek V. Siderophore-based noninvasive differentiation of Aspergillus fumigatus colonization and invasion in pulmonary aspergillosis. Microbiol. Spectr. 2023, 11 (2), e040682210.1128/spectrum.04068-22. PubMed DOI PMC
Patil R. H.; Luptakova D.; Havlicek V. Infection metallomics for critical care in the post-COVID era. Mass Spectrom. Rev. 2023, 42 (4), 1221–1243. 10.1002/mas.21755. PubMed DOI
Bertrand S.; Larcher G.; Landreau A.; Richomme P.; Duval O.; Bouchara J. P. Hydroxamate siderophores of Scedosporium apiospermum. BioMetals 2009, 22 (6), 1019–1029. 10.1007/s10534-009-9253-0. PubMed DOI
Bertrand S.; Bouchara J. P.; Venier M. C.; Richomme P.; Duval O.; Larcher G. Nα-methyl coprogen B, a potential marker of the airway colonization by Scedosporium apiospermum in patients with cystic fibrosis. Med. Mycol. 2010, 48 (O1), S98–S107. 10.3109/13693786.2010.503972. PubMed DOI
Bairwa G.; Hee Jung W.; Kronstad J. W. Iron acquisition in fungal pathogens of humans. Metallomics 2017, 9 (3), 215–227. 10.1039/C6MT00301J. PubMed DOI PMC
Le Govic Y.; Papon N.; Le Gal S.; Lelievre B.; Bouchara J. P.; Vandeputte P. Genomic organization and expression of iron metabolism genes in the emerging pathogenic mold Scedosporium apiospermum. Front. Microbiol. 2018, 9, 827.10.3389/fmicb.2018.00827. PubMed DOI PMC
Le Govic Y.; Papon N.; Le Gal S.; Bouchara J. P.; Vandeputte P. Non-ribosomal peptide synthetase gene clusters in the human pathogenic fungus Scedosporium apiospermum. Front. Microbiol. 2019, 10, 2062.10.3389/fmicb.2019.02062. PubMed DOI PMC
Le Govic Y.; Havlicek V.; Capilla J.; Luptakova D.; Dumas D.; Papon N.; Le Gal S.; Bouchara J. P.; Vandeputte P. Synthesis of the hydroxamate siderophore Nα-methylcoprogen B in Scedosporium apiospermum is mediated by sidD ortholog and is required for virulence. Front. Cell. Infect. Microbiol. 2020, 10, 587909.10.3389/fcimb.2020.587909. PubMed DOI PMC
Luo R.; Zimin A.; Workman R.; Fan Y.; Pertea G.; Grossman N.; Wear M. P.; Jia B.; Miller H.; Casadevall A.; Timp W.; Zhang S. X.; Salzberg S. L. First draft genome sequence of the pathogenic fungus Lomentospora prolificans (formerly Scedosporium prolificans). G3 (Bethesda) 2017, 7 (11), 3831–3836. 10.1534/g3.117.300107. PubMed DOI PMC
Misslinger M.; Hortschansky P.; Brakhage A. A.; Haas H. Fungal iron homeostasis with a focus on Aspergillus fumigatus. Biochim. Biophys. Acta, Mol. Cell Res. 2021, 1868 (1), 118885.10.1016/j.bbamcr.2020.118885. PubMed DOI
Liu H.; Gravelat F. N.; Chiang L. Y.; Chen D.; Vanier G.; Ejzykowicz D. E.; Ibrahim A. S.; Nierman W. C.; Sheppard D. C.; Filler S. G. Aspergillus fumigatus AcuM regulates both iron acquisition and gluconeogenesis. Mol. Microbiol. 2010, 78 (4), 1038–1054. 10.1111/j.1365-2958.2010.07389.x. PubMed DOI PMC
Yap A.; Volz R.; Paul S.; Moye-Rowley W. S.; Haas H. Regulation of high-affinity iron acquisition, including acquisition mediated by the iron permease FtrA, is coordinated by AtrR, SrbA, and SreA in Aspergillus fumigatus. mBio 2023, 14 (3), e007572310.1128/mbio.00757-23. PubMed DOI PMC
Pavlaskova K.; Nedved J.; Kuzma M.; Zabka M.; Sulc M.; Sklenar J.; Novak P.; Benada O.; Kofronova O.; Hajduch M.; Derrick P. J.; Lemr K.; Jegorov A.; Havlicek V. Characterization of pseudacyclins A–E, a suite of cyclic peptides produced by Pseudallescheria boydii. J. Nat. Prod. 2010, 73 (6), 1027–1032. 10.1021/np900472c. PubMed DOI
Krasny L.; Strohalm M.; Bouchara J. P.; Sulc M.; Lemr K.; Barreto-Bergter E.; Havlicek V. Scedosporium and Pseudallescheria low molecular weight metabolites revealed by database search. Mycoses 2011, 54 (s3), 37–42. 10.1111/j.1439-0507.2011.02109.x. PubMed DOI
Novak J.; Lemr K.; Schug K. A.; Havlicek V. CycloBranch: de novo sequencing of nonribosomal peptides from accurate product ion mass spectra. J. Am. Soc. Mass Spectrom. 2015, 26 (10), 1780–1786. 10.1007/s13361-015-1211-1. PubMed DOI
Novak J.; Skriba A.; Havlicek V. CycloBranch 2: molecular formula annotations applied to imzML data sets in bimodal fusion and LC-MS data files. Anal. Chem. 2020, 92 (10), 6844–6849. 10.1021/acs.analchem.0c00170. PubMed DOI
Blin K.; Shaw S.; Augustijn H. E.; Reitz Z. L.; Biermann F.; Alanjary M.; Fetter A.; Terlouw B. R.; Metcalf W. W.; Helfrich E. J. N.; van Wezel G. P.; Medema M. H.; Weber T. antiSMASH 7.0: new and improved predictions for detection, regulation, chemical structures and visualisation. Nucleic Acids Res. 2023, 51 (W1), W46–W50. 10.1093/nar/gkad344. PubMed DOI PMC
Haas H. Iron—a key nexus in the virulence of Aspergillus fumigatus. Front. Microbiol. 2012, 3, 28.10.3389/fmicb.2012.00028. PubMed DOI PMC
Altschul S. F.; Wootton J. C.; Gertz E. M.; Agarwala R.; Morgulis A.; Schaffer A. A.; Yu Y. K. Protein database searches using compositionally adjusted substitution matrices. FEBS J. 2005, 272 (20), 5101–5109. 10.1111/j.1742-4658.2005.04945.x. PubMed DOI PMC
Haas H. Molecular genetics of fungal siderophore biosynthesis and uptake: the role of siderophores in iron uptake and storage. Appl. Microbiol. Biotechnol. 2003, 62 (4), 316–330. 10.1007/s00253-003-1335-2. PubMed DOI
Breci L. A.; Tabb D. L.; Yates J. R. 3rd; Wysocki V. H. Cleavage N-terminal to proline: analysis of a database of peptide tandem mass spectra. Anal. Chem. 2003, 75 (9), 1963–1971. 10.1021/ac026359i. PubMed DOI
Savelieff M. G.; Pappalardo L. Novel cutting-edge metabolite-based diagnostic tools for aspergillosis. PLoS Pathog. 2017, 13 (9), e100648610.1371/journal.ppat.1006486. PubMed DOI PMC
Kostrzewa M. Application of the MALDI Biotyper to clinical microbiology: progress and potential. Expert Rev. Proteomics 2018, 15 (3), 193–202. 10.1080/14789450.2018.1438193. PubMed DOI